Abstract
During maturation, the last phase of oogenesis, the oocyte undergoes several changes which prepare it to be ovulated and fertilized. Immature oocytes are arrested in the first meiotic process prophase, that is morphologically identified by a germinal vesicle. The removal of the first meiotic block marks the initiation of maturation. Although a large number of molecules are involved in complex sequences of events, there is evidence that a calcium increase plays a pivotal role in meiosis re-initiation. It is well established that, during this process, calcium is released from the intracellular stores, whereas less is known on the role of external calcium entering the cell through the plasma membrane ion channels. This review is focused on the functional role of calcium currents during oocyte maturation in all the species, from invertebrates to mammals. The emerging role of specific L-type calcium channels will be discussed.
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Review
Oocyte maturation
Oogenesis is characterized by a unique process of cell division occurring only in gametes, called meiosis; whose goal is the production of haploid cells highly specialized for fertilization. In the majority of species the oocyte arrests in different stages of meiotic division, in particular, the block occurring in the first meiotic prophase (PI) marks the state of immature oocyte characterized by a prominent nucleus called the germinal vesicle (GV), which contains de-condensed transcriptionally active chromatin [[1] for a review]. As a general scheme, in response to a stimulus, meiosis is resumed and manifested by a germinal vesicle breakdown (GVBD), it then progresses to metaphase I (MI) or II (MII) where it undergoes a second arrest that is removed after successful fertilization.
Oocyte maturation is usually defined as the period of progression from the first to the second meiotic arrest and involves coordinated nuclear and cytoplasmic modifications [2]. These are highly complex processes and their interplay is regulated by a series of sequential molecular events. Nuclear maturation starts with the GVBD, ends at the meiosis exit, and is marked by the presence of the two polar bodies. Cytoplasmic maturation is a more obscure process and involves both morphological and functional alterations related to: i) changes in the expression profile of cell cycle control proteins responsible for driving the oocyte towards developmental competencies [3–5]; ii) relocation of organelles [6–8]; iii) transcriptional modifications of mRNA [9], modification of the plasma membrane permeability [10, 11]; iv) the differentiation of the calcium signalling machinery [12].
Although the arrest at the PI stage seems to be strictly correlated with the oocyte growth, the meiotic stage correlated with fertilizable oocyte is species-specific. In some animals, oocytes are fertilized at the PI stage (anellida, plateyhelminthes, polychaeta, mollusca, arthropoda, echinoderms, and some mammals) or, on the contrary, there are some oocytes that are fertilized after meiosis completion (coelenterate, echinoderms). In worms, ascidians, molluscs, and some insects, a second arrest occurs at the MI stage and at the metaphase II (MII) stage in the Amphioxus and all the vertebrates [13, 14] (Fig. 1).
A schematic illustration of the resumption of meiosis in different animal models. The immature oocyte is arrested in prophase I (PI) marked by the germinal vesicle (GV). Depending on the species, oocytes may be fertilized in PI, undergoes a second meiotic block at the metaphase I (MI), metaphase II (MII) or may complete meiosis before fertilization. MII is marked by one polar body (yellow). Resumption from the second meiotic block occurs upon sperm penetration leading to germinal vesicle breakdown (GVBD), meiosis completion and zygote formation marked by the two inner pronuclei and two polar bodies.
The control of oocyte maturation involves a complex interplay between the oocyte and the extracellular membranes and the environment, with the participation of numerous metabolic pathways. The resumption of meiotic maturation relies on two different mechanisms: a positive stimulation and the removal of an inhibitory signal. The former involves the production of a ligand that acts on the oocyte at the GV stage inducing the GVBD. While this general mechanism is common to almost all the species studied, the nature of the ligand that allows the passage between the first and second meiotic block is different in each species.
Studies on this topic have established that 1-methyladenine (1-MA), serotonin, and steroids resume the first meiotic block in starfish [15], molluscs [11, 16], fishes [17], and amphibians [18] respectively, while in mammals, it is the luteinizing hormone (LH) surge [19] that is known for initiating the transition from PI through MI to MII.
In the absence of positive stimulation, meiotic arrest appears to be maintained by a constraint of the environment surrounding the oocyte. In some species, oocytes undergo maturation as soon as they are isolated from their follicles or the external milieu, suggesting that these elements contain substances preventing meiosis resumption of PI arrested oocytes [20, 21]. Assuming the existence of an interplay between the two mentioned mechanisms, meiosis resumption may occur through: i) the generation of a signal that in turn is transferred to the oocyte through the follicular environment; ii) the override of the environmental inhibition by removing the contact between oocyte and its follicular envelope and the closure of the connecting junctions [22].
Meiosis arrest and resumption are modulated by numerous messengers. Many studies have provided evidence of the involvement of cyclic nucleotides in the maintenance of meiotic arrest [23]. Elevated levels of cyclic adenosine mono-phosphate (cAMP), some analogues, cAMP-dependent protein kinase (PKA), and related substances such as GPR3, act by preventing spontaneous maturation and/or blocking GVBD in vitro [24–28]. However, contrasting data show that high levels of cAMP may only transiently block GVBD [29] or may even release the oocyte from meiotic arrest. [30, 31].
Another important factor responsible for meiosis resumption is the M-phase promoting factor (MPF) showed for the first time in amphibian oocytes in the 70s, by Masui [32]. Nonetheless most of the work on MPF has been carried out with frog and starfish oocytes, accumulated evidence demonstrates that this complex function exists in other animal models, such as mammals and invertebrates [10, 33–36] . Although oocytes from different species display different sensitivities to inhibitory and stimulatory ligands, there is a general consensus that calcium ions play a fundamental role in the resumption of meiotic maturation [4, 37].
Review of the literature concerning the types of calcium currents involved in meiotic transition stages in oocytes of different animal models. Intracellular calcium currents may be mediated by IP3, Ryanodine (Ry), or cyclic ADP ribose. Plasma membrane calcium currents may be mediated by unspecific or L-type channels. Capacitative is the interplay mechanism that links plasma membrane and intracellular currents.
Calcium and maturation
The role of ion currents in the oocyte physiology is described in many animal species [38–41]. In particular, calcium currents have been shown to be vital in regulating a broad range of physiological processes [42, 43].
The calcium rise in the cell occurs by means of two principal mechanisms: the efflux from the stores via ligand-gated channels on organelle membranes, and the entry through ion channels in the plasma membrane. Most of the events underlined by the former mechanism are associated with two families of ion channels stored in the endoplasmic and/or sarcoplasmic reticulum in all cell types: the ryanodine receptor (Ryr) and the inositol 1,4,5-trisphosphate receptors (IP3r). The phosphoinositide pathway is of primary importance in mobilizing calcium into the cell, since elevation of IP3 levels elicits transient calcium currents from the intracellular stores [44, 45]. On the other hand, calcium ionophore, is known to cause an increase in intracellular calcium concentration through Ryr. IP3 and Ry receptor/channels complexes share common features for what concerns both the amplification of calcium release by a positive feedback and the termination due to a negative feedback [46]. The responsiveness of the intracellular receptors/channels is regulated by a combination of factors, such as the calcium loading of the reticulum, and the sensitivity of the receptors to cytosolic calcium and to agonist concentration [46]. In excitable tissues, calcium entry is accomplished by the opening of voltage-operated calcium channels (VOCs) that mediate calcium influx in response to membrane depolarization [47]. At last, a connection between the two pathways is supported by the store-operated channels [48] through which a calcium influx is induced by the depletion of internal stores [49].
It is well established that calcium is involved in the physiology of the oocyte from oogenesis to maturation and fertilization [33, 50–53]. Particularly, it has been described that the transition from one meiotic phase to the following is regulated by cell cycle control checkpoints which are in turn modulated by a transient increase of intracellular calcium in many animal species [4]. A general correlation between calcium and the GVBD has been demonstrated by a large number of studies. GVBD in mammalian oocytes is blocked by calcium chelators at least up to the first metaphase [33] whereas, in absence of intracellular calcium elevation spontaneous meiosis resumption in vitro does not occur [54]. Consistent data showed that injection of calcium in mouse oocytes induces parthenogenetic activation and subsequent normal development [55].
Intracellular and plasma membrane calcium currents
Literature reveals that re-initiation of meiosis is mediated by both intracellular and plasma membrane calcium currents, sometimes in a synergic cooperation. In some species, intracellular currents stimulated by calcium ionophore induce oocyte maturation [56, 57] whereas, particularly in starfish, it appears that IP3r amounts and sensitivity to IP3 increase during maturation. Although a direct correlation between GVBD and calcium internal currents has not been proven in this species [58], there is evidence that in the maturing oocyte the mechanism for calcium release is mediated also by Ry and cADP-ribose sensitive channels [7, 59–61].
In molluscs in 1953, Allen [62] first reported a role of external calcium in the induction of GVBD in the Spisula. Later on, the external calcium requirement through voltage-gated channels was confirmed in this species and extended to the other molluscs that are also fertilized at the PI stage [63, 64], or undergo the second arrest in MI [11, 65]. Along with the extracellular calcium induction of GVBD in molluscs, it was soon recognized that there was an influence of the intracellular calcium elevation in almost all species studied independently from their peculiar meiotic arrest [64, 66, 67]. In particular, the interplay between external and internal calcium currents is evident in Ruditapes; here, a serotonin-induced surge of intracellular calcium was shown to trigger maturation even in the absence of external calcium [67]. As a general rule in molluscs, the initial plasma membrane calcium currents create a depolarization that, in turn, mobilize intracellular calcium currents from the stores [16, 68]. However, a few exceptions must be mentioned, such as the Hiatella flaccida, where an intracellular calcium increase might be responsible for release from PI arrest, without a correlation with extracellular calcium [69]. Another example is the oyster [70], where calcium might not be involved in the early maturational stages. In surf clams and bivalves, experiments with IP3-induced GVBD suggest that release of internal calcium may be mediated by IP3-sensitive calcium currents [68, 69, 71, 72].
Ascidians are ubiquitous marine invertebrates, whose oocytes maturate in the ovary. Immature oocytes are characterized by the GV; subsequently, to a still unknown stimulus, they undergo GVBD and resume meiosis up to the MI mature stage. Despite a large number of studies on ascidians, little information is available on the mechanisms that induce oocyte passage from the PI to MI block [73]. Very recently, Lambert [74] reviewed the signalling pathways underlying GVBD and he indicated that in some species the calcium ionophore induces GVBD [75]. In addition, it has been shown that intracellular calcium may either trigger or inhibit the GVBD onset [76]. Although these data show a general calcium role, a specific involvement of ion currents has been examined only recently in the ascidian Ciona intestinalis. Here, the first electrophysiological characterization of the plasma membrane at the GV stage oocytes – along with in vitro maturation experiments – strongly indicate a role of voltage-gated calcium currents in the prophase/metaphase transition [77].
Oocyte maturation mechanisms have been described in amphibians since the mid 80s [78]. Ion currents have been widely examined in immature oocytes of Xenopus laevis and Rana esculenta with growing evidence that chloride currents play a relevant role in the physiology of the oocyte [39]. Literature of the late 70s reports that transient calcium rises were associated to steroid-induced maturation events [79, 80] proposing calcium function as the initial step in maturation induction. Although contrasting results indicated that calcium itself was not necessary to Xenopus oocyte maturation [81], recently Machaca [12] demonstrated a direct action of calcium release events during oocyte maturation in this species. Actually, evidence exists for an involvement of calcium currents in the activation of chloride [82–85], sodium, and hydrogen currents [86, 87].
In amphibians, apart from a general change of membrane permeability during maturation [88], it seems that nobody has thus far correlated meiosis progression and/or GVBD to the intracellular or plasma membrane calcium current activity. However, when a role for ion calcium release in immature oocytes was shown, evidence demonstrated that this event occurs through IP3-sensitive stores currents [12, 84, 86, 87].
In mammals, as a general scheme, oocyte maturation involves the resumption of meiosis in response to a surge of LH [23], the disruption of gap junctions after gonadotropin stimulation [89] and a decrease in cAMP levels [23]. Although a potential role of calcium currents in meiosis resumption is known, it remains to be elucidated if: i) calcium participates by itself as positive signal by coupling LH-induced GVBD or, ii) the other factors that traverse the gap junctions may influence the calcium levels within the oocyte. Literature shows that intracellular calcium oscillation is required for spontaneous maturation of mouse [90, 91] and pig [92] oocytes, and that the increase in calcium concentrations at the time of GVBD confirms the relationship between intracellular calcium currents and oocyte maturation in different species [54, 90, 92, 93]. The occurrence of spontaneous calcium oscillations in the mouse GV oocyte during meiotic maturation in vitro showed the involvement of an IP3-dependent mechanism [94], such as in hamsters [95], bovine [96], and humans [97].
Along with IP3 receptors and nonetheless many controversies, the occurrence of functional Ryr suggested an additional Ry-sensitive calcium-release mechanism in mouse [[55] and references therein], bovine [98], and human GV oocytes [99]. All together these data indicate that GV mammalian oocytes may account for both IP3 and Ry-mediated intracellular calcium currents in the meiotic transition from PI to MII stage.
Similar data have been reported for plasma membrane calcium currents; in fact the occurrence of both not-specific and calcium channels on the immature oocyte plasma membrane of mammals were demonstrated by Yoshida [100–102], whereas an externally derived calcium requirement at maturation was shown in the hamster [57] and other mammals [56, 103–105].
In 1993, Murnane and De Felice [106] performed the first accurate electrophysiological characterization of immature murine oocytes demonstrating that plasma membrane calcium currents selectively increase in the growing oocyte and that this increase precedes nuclear maturation. These authors suggested that either intracellular or plasma membrane calcium currents may mediate the onset of oocyte maturation. In mice, confirming findings showed that GV and GVBD-arrested oocytes had some defects in calcium channel expression or translation, suggesting that an increase of calcium channel density may attain the oocyte meiotic competence [107].
The first electrophysiological characterization of GV stage bovine oocytes showed a plasma membrane calcium current activity during meiotic progression [108] and a prevalence of calcium stores at the GV stage [109]. Together these data indicated a possible association between LH-mediated calcium elevation and plasma membrane calcium currents. It was, in fact, suggested that in addition to store-released calcium, the plasma membrane currents might provide an alternative/additional mode of calcium entry in meiosis resumption. As it happens with bovine, recent preliminary experiments in sheep oocyte plasma membrane showed an involvement of calcium currents in the GV/MII transition [110]. Despite the general consensus, a few conflicting data show that calcium ion transport may underlie only a few phases of maturation [111] and even a calcium-independent GVBD in the mouse [112].
L-type calcium currents
Numerous studies indicate that the intracellular calcium release is the universal mechanism that underlies the meiotic resumption at oocyte maturation [33, 51]. On the contrary, the involvement of plasma membrane calcium currents has been described only in some species of molluscs [11, 113–115], ascidians [77], amphibians [117], and mammals [106–108]. It is interesting that, in many cases, the specific channels involved in meiosis re-initiation are L-type calcium channels. These are voltage-gated channels that open in response to a depolarization of the plasma membrane and are expressed in different tissues in order to mediate signalling between cell membrane and intracellular processes, i.e. blood pressure regulation, smooth muscle contractility, insulin secretion, cardiac development, and learning and memory [[118], for a review]. In ascidians it was recently demonstrated that L-type calcium channels are involved in a series of biological processes [119]; however, first indication of a role of these channels in the reproductive processes was provided in mature oocytes [120, 121], suggesting that cytosolic calcium release may be modulated by these plasma membrane calcium currents. Similarly, in some molluscs, progressive appearance of L-type calcium currents after stimulation by 5-HT correlated with the ability of MI-arrested oocytes seems to be responsive to fertilization [114, 115]. Only in recent years has it been found that, in different species, oocyte maturation marked by the GVBD relies specifically on L-type calcium currents. In the mollusc this occurs in species with diverse maturational behaviour. In telolecitic oocytes of Octopus vulgaris maturation was strictly correlated with the decline in L-type calcium currents and the different developmental stages of cytoplasmic and nuclear maturation [11] and in the mussel oocytes a perfect correlation between inhibition of plasma membrane L-type calcium channels and inhibition of meiosis was shown [115]. In addition, in the Mytilus these channels appeared to be essential to sustain cytosolic calcium increase in order to extrude the first polar body.
A supporting finding also comes from the amphibians. Pleurodeles oocyte maturation is responsive to progesterone stimulation only during the breeding season versus a resting season. Interestingly, an electrophysiological study has strictly correlated the alternate expression of calcium channels in the two seasons, showing a higher current density and functional expression of the L-type during the maturational period. Furthermore, this study demonstrated a clear correlation of L-type calcium channel activity, cAMP levels, and the inability of the oocyte to mature [117]. In the ascidian Ciona intestinalis [77] the electrical characterization of the GV stage plasma membrane was recently carried out showing the higher occurrence of L-type calcium channels in the GV with respect to the mature stage. This pattern, together with the higher intracellular calcium release in the MI oocyte, has led to the hypothesis that L-type channels may play a double role in both regulating the GV/MI transition and participating in the loading of calcium stores necessary for subsequent fertilization. Similarly, the ability to reduce the GVBD in absence of external calcium further suggests that this response may require functional plasma membrane calcium channels [77].
Substantial differences occur in mammalian species. In the mouse it was first shown that the external calcium dependence implies the involvement of unspecific voltage-gated calcium channels in the onset of maturation in the different developmental stages such as oocytes-neonatal and GV stages [106]. However, a clear distribution pattern of the L-type calcium channels has only been subsequently provided showing that they undergo a density rearrangement only in the later stages of maturation until disappearing totally at the blastocyst stage [107].
Recently a significant distributional change of the L-type calcium channels activity from the GV to the MII stage was identified in bovine and ovine oocytes [108, 110]. The results suggest that a possible common mechanism for the maturation starting in these two species is the calcium entry through specific channels potentiating the physiological oocyte-cumulus signalling responsible for meiotic awakening and progression.(Fig. 2)
Conclusion
The evidence presented in this review supports the hypothesis that voltage-gated calcium ion currents are involved in the increase of cytosolic calcium levels occurring at oocyte maturation. Specific focus is centred on the occurrence and the pattern of L-type calcium currents during PI/metaphase transition in different animal species, implying that expression and translation of these types of calcium channels may be essential requirements for the oocyte maturation process and normal development. In vitro maturation of human oocytes is a challenge that could revolutionize the infertility treatment and IVF procedures. In this respect, future research will hopefully lead to determining the complex interplay between calcium current dynamics and other metabolic pathways participating in oocyte maturation aimed at successful oocyte fertilization and developmental competence.
References
Voronina E, Wessel GM: The regulation of oocyte maturation. Curr Top Dev Biol. 2003, 58: 53-110.
Eppig JJ: Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev. 1996, 8: 485-489. 10.1071/RD9960485.
Masui Y: A quest for cytoplasmic factors that control the cell cycle. Prog Cell Cycle Res. 1996, 2: 1-13.
Whitaker M, Patel R: Calcium and cell cycle control. Development. 1990, 108: 525-542.
Whitaker M: Control of meiotic arrest. Rev Repr. 1996, 1: 127-135. 10.1530/ror.0.0010127.
Ducibella TA, Anderson DF, Albertini F, Aalberg J, Rangarajan S: Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during maturation. Dev Biol. 1988, 130: 184-197. 10.1016/0012-1606(88)90425-3.
Santella L, De Riso L, Gragnaniello G, Kyozuka K: Cortical granule translocation during maturation of starfish oocytes requires cytoskeletal rearrangement triggered by InsP3-mediated Ca2+ release. Exp Cell Res. 1999, 248: 567-574. 10.1006/excr.1999.4425.
Wessel GM, Brooks JM, Green E, Haley S, Voronina E, Wong J, Zaydfudim V, Conner S: The biology of cortical granules. Int Rev Cytol. 2001, 209: 117-206.
Hake LE, Richter JD: Translational regulation of maternal mRNA. Biochem Biophys Acta. 1997, 1332: M31-M38.
Carroll J: Na+-Ca2+ exchange in mouse oocytes: modifications in the regulation of intracellular free Ca2+ during oocyte maturation. J Reprod Fert. 2000, 118: 337-342. 10.1530/reprod/118.2.337.
Cuomo A, Di Cristo C, Di Cosmo A, Paolucci M, Tosti E: Calcium currents correlate with oocyte maturation during the reproductive cycle in Octopus vulgaris. J Exp Zool A. 2005, 303: 193-202. 10.1002/jez.a.152.
Machaca K: Increased sensitivity and clustering of elementary Ca2+ release events during oocyte maturation. Dev Biol. 2004, 275: 170-182. 10.1016/j.ydbio.2004.08.004.
Thibault C: Formation et maturation des gametes. Traitè de Zoologie: Anatomie, Systematique, Biologie. Edited by: Grasse PP. 1969, Paris Masson et Cie, 16: 799-853.
Masui Y: Meiotic arrest in animal oocytes. Biology of Fertilization. Edited by: Metz CB, Monroy A. 1985, New York: Academic Press, 1: 189-219.
Mita M: 1 – Methyiladenine: a starfish oocyte maturation-inducing substance. Zygote. 2000, 8S: 9-11.
Colas P, Dubé F: Meiotic maturation in mollusc oocytes. seminars in Cell & Dev Biol. 1998, 9: 539-548. 10.1006/scdb.1998.0248.
Iwamatsu T, Toya Y, Sakai N, Terada Y, Nagata R, Nagahama Y: Effect of 5-Hydroxytryptamine on steroidogenesis and oocyte maturation in pre-ovulatory follicles of the medaka Oryzias latipes. Develop Growth & Differ. 1993, 35: 625-630. 10.1111/j.1440-169X.1993.00625.x.
Schorderet-slatkine S: Action of progesterone and related steroids on oocyte maturation in Xenopus laevis. An in vitro study. Cell Differ. 1972, 1: 179-189. 10.1016/0045-6039(72)90027-9.
Moor RM, Osborne JC, Cran DG, Walters DE: Selective effect of gonadotropins on cell coupling, nuclear maturation, and protein synthesis in mammalian oocytes. J Embryol Exp Morphol. 1981, 61: 347-365.
Edwards RG: Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965, 208: 349-351.
Tsafriri A, Pomerantz SH: Oocyte maturation inhibitor. Clin Endocrinol Metab. 1986, 15: 157-170. 10.1016/S0300-595X(86)80047-0.
Eppig JJ: Intercommunication between mammalian oocytes and companion somatic cells. Bioessays. 1991, 13: 569-574. 10.1002/bies.950131105.
Eppig JJ, Downs SM: Chemical signals that regulate mammalian oocyte maturation. Biol Reprod. 1984, 30: 1-11. 10.1095/biolreprod30.1.1.
Schultz RM: Molecular aspects of mammalian oocyte growth and maturation. Experimental Approaches to mammalian Embryonic Development. Edited by: Rossant J, Pederson RA. 1986, Cambridge: Cambridge University Press, 195-237.
Conti M, Andersen CB, Richard FJ, Shitsukawa K, Tsafriri A: Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol Cell Endocrinol. 1998, 145: 9-14. 10.1016/S0303-7207(98)00187-7.
Yoshimura Y, Nakamura Y, Oda T, Ando M, Ubukata Y, Karube M, Koyama N, Yamada H: Induction of meiotic maturation of follicle-enclosed oocytes of rabbits by a transient increase followed by an abrupt decrease in cyclic AMP concentration. J Reprod Fert. 1992, 95: 803-812.
Mehlmann LM: Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev Biol. 2005, 288: 397-404. 10.1016/j.ydbio.2005.09.030.
Freudzon L, Norris RP, Hand AR, Tanaka S, Saeki Y, Jones TL, Rasenick MM, Berlot CH, Mehlmann LM, Jaffe LA: Regulation of meiotic prophase arrest in mouse oocytes by GPR3, a constitutive activator of the Gs G protein. J Cell Biol. 2005, 171: 255-265. 10.1083/jcb.200506194.
Sirard MA, First NL: In vitro inhibition of oocyte nuclear maturation in the bovine. Biol Reprod. 1988, 39: 229-234. 10.1095/biolreprod39.2.229.
Stricker SA, Smythe TL: 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms. Development. 2001, 128: 1415-1427.
Yi JH, Lefievre L, Gagnon C, Anctil M, Dube F: Increase of cAMP upon release from prophase arrest in surf clam oocytes. J Cell Sci. 2002, 115: 311-320.
Masui Y: From oocyte maturation to the in vitro cell cycle: the history of discoveries of Maturation-Promoting Factor (MPF) and Cytostatic Factor (CSF). Differentiation. 2001, 69: 1-17. 10.1046/j.1432-0436.2001.690101.x.
Homa S: Calcium and meiotic maturation of the mammalian oocyte. Mol Repr Dev. 1995, 40: 122-134. 10.1002/mrd.1080400116.
Russo GL, Kyozuka K, Antonazzo L, Tosti E, Dale B: Maturation promoting factor in ascidian oocytes is regulated by different intracellular signals at meiosis I and II. Development. 1996, 122: 1995-2003.
Kishimoto T: Cell cycle arrest and release in starfish oocytes and eggs. seminars in Cell & Dev Biol. 1998, 9: 549-557. 10.1006/scdb.1998.0249.
Yamashita M, Mita K, Yoshida N, Kondo T: Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects. Prog Cell Cycle Res. 2000, 4: 115-129.
Whitaker M: Calcium at fertilization and in early development. Physiol Rev. 2006, 86: 25-88. 10.1152/physrev.00023.2005.
Hagiwara S, Jaffe LA: Electrical properties of egg cell membranes. Annu Rev Biophys Bioeng. 1979, 8: 385-416. 10.1146/annurev.bb.08.060179.002125.
Schlichter LC: Ionic currents underlying the action potential of Rana pipiens. Dev Biol. 1989, 134: 59-71. 10.1016/0012-1606(89)90078-X.
Moody WJ: The development of voltage-gated ion channels and its relation to activity-dependent development events. Curr Top Dev Biol. 1998, 39: 159-185.
Tosti E, Boni R: Electrical events during gamete maturation and fertilisation in animals and human. Hum Reprod Update. 2004, 10: 53-65. 10.1093/humupd/dmh006.
Carafoli E: Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA. 2002, 99: 1115-1122. 10.1073/pnas.032427999.
Berridge MJ, Bootman MD, Roderick HL: Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003, 4: 517-529. 10.1038/nrm1155.
Berridge MJ: Inositol trisphosphate and calcium signalling. Nature. 1993, 361: 315-325. 10.1038/361315a0.
Pozzan T, Rizzuto R, Volpe P, Meldolesi J: Molecular and cellular physiology of intracellular calcium stores. Physiol Rev. 1994, 74: 595-636.
Bootman MD, Berridge MJ: The elemental principles of calcium signalling. Cell. 1995, 83: 675-678. 10.1016/0092-8674(95)90179-5.
Catteral WA: Structure and regulation of voltage-gated Ca2+ channels. Ann Rev Cell and Dev Biol. 2000, 16: 521-555. 10.1146/annurev.cellbio.16.1.521.
Parekh AB: Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol. 2003, 547: 333-348. 10.1113/jphysiol.2002.034140.
Putney JW: Capacitative calcium entry revisited. Cell Calcium. 1990, 11: 611-624. 10.1016/0143-4160(90)90016-N.
Homa ST, Carroll J, Swann K: The role of calcium in mammalian oocyte maturation and egg activation. Hum Repr. 1993, 8: 1274-1281.
Carroll J, Jones KT, Whittingham D: Ca2+ release and the development of Ca2+ release mechanisms during oocyte maturation: a prelude to fertilization. Rev Reprod. 1996, 1: 137-143. 10.1530/ror.0.0010137.
Whitaker M, Swann K: Lighting the fuse at fertilization. Development. 1993, 117: 1-12.
Stricker SA: Comparative biology of calcium signalling during fertilization and egg activation in animals. Dev Biol. 1999, 211: 157-176. 10.1006/dbio.1999.9340.
Carroll J, Swann K, Whittingham D, Whitaker M: Spatiotemporal dynamics of intracellular [Ca2+]i oscillations during the growth and meiotic maturation of mouse oocytes. Development. 1994, 120: 3507-3517.
Jones KT, Carroll J, Whittingham DG: Ionomycin, thapsigargin, ryanodine, and sperm induced Ca2+ release increase during meiotic maturation of mouse oocytes. J Biol Chem. 1995, 270: 6671-6677. 10.1074/jbc.270.12.6671.
Powers RD, Paleos GA: The combined effects of Ca and dibutyryl cyclic AMP on germinal vesicle breakdown in the mouse oocyte. J Reprod Fert. 1982, 66: 1-8.
Racowsky C: The releasing action of calcium upon cyclic AMP-dependent meiotic arrest in hamster oocytes. J Exp Zool. 1986, 239: 263-275. 10.1002/jez.1402390214.
Witchel HJ, Steinhardt RA: 1-Methyladenine can consistently induce a fura-detectable transient calcium increase which is neither necessary nor sufficient for maturation in oocytes of the starfish Asterina miniata. Dev Biol. 1990, 141: 393-398. 10.1016/0012-1606(90)90393-W.
Chiba K, Kado RT, Jaffe LA: Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol. 1990, 140: 300-306. 10.1016/0012-1606(90)90080-3.
Stricker SA, Centonze VE, Melendez RF: Calcium dynamics during starfish oocyte maturation and fertilization. Dev Biol. 1994, 166: 34-58. 10.1006/dbio.1994.1295.
Iwasaki H, Chiba K, Uchiyama T, Yoshikawa F, Suzuki F, Ikeda M, Furuichi T, Mikoshiba K: Molecular characterization of the starfish inositol 1,4,5-trisphosphate receptor and its role during oocyte maturation and fertilization. J Biol Chem. 2002, 277: 2763-2772. 10.1074/jbc.M108839200.
Allen RD: Fertilization and artificial activation in the egg of the surf clam, Spisula solidissima. Biol Bull. 1953, 105: 213-239.
Dubé F: The relationships between early ionic events, the pattern of protein syntesis, and oocyte activation in the surf clam, Spisula solidissima. Dev Biol. 1988, 126: 233-241. 10.1016/0012-1606(88)90134-0.
Deguchi R, Osanai K: Meiosis reinitiation from the first prophase is dependent on the levels of intracellular Ca2+ and pH in oocytes of the bivalves Mactra chinensis and Limaria hakodatensis. Dev Biol. 1994, 166: 587-599. 10.1006/dbio.1994.1339.
Dubé F, Guerrier P: Activation of Barnea candida (Mollusca, Pelecypoda) oocytes by sperm or KCl, but not by NH4 Cl, requires a calcium influx. Dev Biol. 1982, 92: 408-417. 10.1016/0012-1606(82)90186-5.
Juneja R, Ito E, Koide SS: Effect of serotonin and tricyclic antidepressants on intracellular calcium concentrations in Spisula oocytes. Cell Calcium. 1994, 15: 1-6. 10.1016/0143-4160(94)90099-X.
Guerrier P, Leclerc-David C, Moreau M: Evidence for the involvement of internal calcium stores during serotonin-induced meiosis reinitation in oocytes of the bivalve mollusc Ruditapes philippinarum. Dev Biol. 1993, 159: 474-484. 10.1006/dbio.1993.1257.
Deguchi R, Morisawa M: External Ca2+ is predominantly used for cytoplasmic and nuclear Ca2+ increases in fertilized oocytes of the marine bivalve Mactra chinensis. J Cell Sci. 2003, 116: 367-376. 10.1242/jcs.00221.
Deguchi R, Osanai K: Serotonin-induced meiosis reinitiation from the first prophase and from the first metaphase in oocytes of the marine bivalve Hiatella flaccida: respective changes in intracellular Ca2+ and pH. Dev Biol. 1995, 171: 483-496. 10.1006/dbio.1995.1298.
Kyozuka K, Deguchi R, Yoshida N, Yamashita M: Change in intracellular Ca2+ is not involved in serotonin-induced meiosis reinitiation from the first prophase in oocytes of the marine bivalve Crassostrea gigas. Dev Biol. 1997, 182: 33-41. 10.1006/dbio.1996.8470.
Bloom TL, Szuts EZ, Eckberg WR: Inositol trisphosphate, inositol phospholipid metabolism, and germinal vesicle breakdown in surf clam oocytes. Dev Biol. 1988, 159: 474-484.
Guerrier P, Durocher Y, Gobet I, Leclerc C, Moreau M: Reception and transduction of the serotonin signal responsible for oocyte meiosis reinitiation in bivalves. Inv Reprod Dev. 1996, 30: 39-45.
Russo GL, Wilding M, Marino M, Dale B: Ins and outs of meiosis in ascidians. seminars in Cell Dev Biol. 1998, 9: 559-567. 10.1006/scdb.1998.0250.
Lambert CC: Signalling pathways in ascidian oocyte maturation: effects of various inhibitors and activators on germinal vesicle breakdown. Dev Growth Differ. 2005, 47: 265-272. 10.1111/j.1440-169X.2005.00796.x.
Sakairi K, Shirai H: Possible MS production by follicle cells in spontaneous oocyte maturation of the ascidian, Halocynthia roretzi. Dev Growth Differ. 1991, 33: 155-162. 10.1111/j.1440-169X.1991.00155.x.
Sun L, Machaca K: Ca2+cyt negatively regulates the initiation of oocyte maturation. J Cell Biol. 2004, 165: 63-75. 10.1083/jcb.200309138.
Cuomo A, Silvestre F, De Santis R, Tosti E: Ca2+ and Na+ current patterns during oocyte maturation, fertilization and early developmental stages of Ciona intestinalis. Mol Reprod Dev. 2006, 73: 501-511. 10.1002/mrd.20404.
Maller JL: Oocyte maturation in amphibians. Dev Biol. 1985, 1: 289-311.
Baulieu EE, Godeau F, Schorderet M, Schorderet-Slatkine S: Steroid-induced meiotic division in Xenopus laevis oocytes: surface and calcium. Nature. 1978, 275: 593-598. 10.1038/275593a0.
Moreau M, Vilain JP, Guerrier P: Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol. 1980, 78: 201-214. 10.1016/0012-1606(80)90329-2.
Cork RJ, Cicirelli MF, Robinson KR: A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. Dev Biol. 1987, 121: 41-47. 10.1016/0012-1606(87)90136-9.
Barish ME: A transient calcium-dependent chloride current in the immature Xenopus oocyte. J Physiol. 1983, 342: 309-325.
Toselli M, Taglietti V, Tanzi F, D'Angelo E: Calcium-dependent chloride transient currents in the immature oocyte of the frog, Rana esculenta. Arch Ital Biol. 1989, 127: 69-80.
Ferguson JE, Han JK, Kao JP, Nuccitelli R: The effects of inositol trisphosphates and inositol tetrakisphosphate on Ca2+ release and Cl- current pattern in the Xenopus laevis oocyte. Exp Cell Res. 1991, 192: 352-365. 10.1016/0014-4827(91)90052-V.
Ivorra I, Morales A: Membrane currents in immature oocytes of the Rana perizi frog. Pflűgers Archiv. 1997, 434: 413-421. 10.1007/s004240050415.
Charpentier G: Induction of membrane excitability in Xenopus oocytes. J Soc Biol. 1999, 193: 517-522.
Humez S, Collin T, Matifat F, Guilbault P, Fournier F: InsP3-dependent Ca2+ oscillations linked to activation of voltage-dependent H+ conductance in Rana esculenta oocytes. Cell Signal. 1996, 8: 375-379. 10.1016/0898-6568(96)00082-4.
Lau YT, Reynhout JK, Horowitz SB: Membrane permeability changes during Rana oocyte maturation. Experientia. 1994, 50: 606-609. 10.1007/BF01921732.
Gilula NB, Epstein ML, Beers WH: Cell-to-cell communication and ovulation. J Cell Biol. 1978, 78: 58-75. 10.1083/jcb.78.1.58.
De Felici M, Dolci S, Siracusa G: An increase of intracellular free Ca2+ is essential for spontaneous meiotic resumption by mouse oocytes. J Exp Zool. 1991, 260: 401-405. 10.1002/jez.1402600314.
Carroll J, Swann K: Spontaneous cytosolic calcium oscillations driven by inositol triphosphate occur during in vitro maturation of mouse oocyte. J Biol Chem. 1992, 267: 11196-11210.
Kaufman ML, Homa ST: Defining a role for calcium in the resumption and progression of meiosis in the pig oocyte. J Exp Zool. 1993, 265: 69-76. 10.1002/jez.1402650110.
Batta SK, Knudsen JF: Calcium concentration in cumulus enclosed oocytes of rats after treatment with pregnant mares serum. Biol Reprod. 1980, 22: 243-246. 10.1095/biolreprod22.2.243.
Deng MQ, Huang XY, Tang TS, Sun FZ: Spontaneous and fertilization-induced Ca2+ oscillations in mouse immature germinal vesicle-stage oocytes. Biol Reprod. 1998, 58: 807-813. 10.1095/biolreprod58.3.807.
Fujiwara T, Nakada K, Shirakawa H, Miyazaki S: Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Dev Biol. 1993, 156: 69-79. 10.1006/dbio.1993.1059.
He Cl, Damiani P, Parys JB, Fissore RA: Calcium, calcium release receptors, and meiotic resumption in bovine oocytes. Biol Reprod. 1997, 57: 1245-1255. 10.1095/biolreprod57.5.1245.
Goud PT, Goud AP, Van Oostveldt P, Dhont M: Presence and dynamic redistribution of type I inositol 1,4,5-trisphosphate receptors in human oocytes and embryos during in-vitro maturation, fertilization and early cleavage divisions. Mol Hum Reprod. 1999, 5: 441-451. 10.1093/molehr/5.5.441.
Tosti E, Boni R, Cuomo A: Fertilization and activation currents in bovine oocytes. Reproduction. 2002, 124: 835-846. 10.1530/rep.0.1240835.
Balakier H, Dziak E, Sojecki A, Librach C, Michalak M, Opas M: Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos. Hum Reprod. 2002, 17: 2938-2947. 10.1093/humrep/17.11.2938.
Yoshida S: Na and Ca spikes produced by ions passing through Ca channels in mouse ovarian oocytes. Pflugers Arch. 1982, 395: 84-86. 10.1007/BF00584975.
Yoshida S: Permeation of divalent and monovalent cations through the ovarian oocyte membrane of the mouse. J Physiol (Lond). 1983, 339: 631-642.
Peres A: Resting membrane potential and inward current properties of mouse ovarian oocytes and eggs. Pflugers Arch. 1986, 407: 534-540. 10.1007/BF00657512.
Preston SL, Parmer TG, Behrman HR: Adenosine reverses Ca-dependent inhibition of follicle-stimulating hormone action and induction of maturation in cumulus enclosed rat oocytes. Endocrinology. 1987, 120: 1356-1364.
Goron S, Oron Y, Dekel N: Rat oocyte maturation: role of calcium in hormone action. Mol Cell Endocrinol. 1990, 72: 131-138. 10.1016/0303-7207(90)90103-F.
Mattioli M, Barboni B: Signal transduction mechanism for LH in the cumulus-oocyte complex. Mol Cell Endocrinol. 2000, 161: 19-23. 10.1016/S0303-7207(99)00218-X.
Murnane JM, De Felice LJ: Electrical maturation of murine oocytes: an increase in calcium current coincides with acquisition of meiotic competence. Zygote. 1993, 1: 49-60.
Lee JH, Yoon SY, Bae IH: Studies on Ca2+-channel distribution in maturation arrested mouse oocyte. Mol Reprod Dev. 2004, 69: 174-185. 10.1002/mrd.20162.
Tosti E, Boni R, Cuomo A: Ca2+ current activity decreases during meiotic progression in bovine oocytes. Am J Physiol – Cell Physiol. 2000, 279: C1795-C1800.
Boni R, Cuomo A, Tosti E: Developmental potential in bovine oocytes is related to cumulus-oocyte complex (COC) grade, calcium current activity and calcium stores. Biol Reprod. 2002, 66: 836-842. 10.1095/biolreprod66.3.836.
Boni R, Cocchia N, Silvestre F, Tortora G, Lorizio R, Tosti E: Plasma membrane electrical properties and intracellular calcium stores in immature and in vitro-matured adult and juvenile sheep oocytes [abstract]. Repr Fert Dev. 2005, 17: s279-10.1071/RDv17n2Ab259.
Igusa Y, Miyazaki S, Yamashita N: Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm. J Physiol. 1983, 340: 633-647.
Tombes RM, Simerly C, Borisy GG, Schatten G: Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca2+ whereas germinal vesicle breakdown is Ca2+ independent in the mouse oocyte. J Cell Biol. 1992, 117: 799-811. 10.1083/jcb.117.4.799.
Dubè F: Thapsigargin induces meiotic maturation in surf clam oocytes. Biochem Biophys Res Commun. 1992, 189: 79-84. 10.1016/0006-291X(92)91528-X.
Moreau M, Leclerc C, Guerrier P: Meiosis reinitiation in Ruditapes philippinarum (Mollusca): involvement of L-calcium channels in the release of metaphase I block. Zygote. 1996, 4: 151-157.
Tomkowiak M, Guerrier P, Krantic S: Meiosis reinitiation of mussel oocytes involves L-type voltage-gated calcium channel. J Cell Biochem. 1997, 64: 152-160. 10.1002/(SICI)1097-4644(199701)64:1<152::AID-JCB17>3.0.CO;2-N.
Leclerc C, Guerrier P, Moreau M: Role of dihydropyridine-sensitive calcium channels in meiosis and fertilization in the bivalve molluscs Ruditapes philippinarum and Crassostrea gigas. Biol Cell. 2000, 92: 285-299. 10.1016/S0248-4900(00)01069-8.
Ouadid-Ahidouch H: Voltage-gated calcium channels in Pleurodeles oocytes: classification, modulation and functional roles. Zygote. 1998, 6: 85-95. 10.1017/S096719949800001X.
Moosmang S, Lenhardt P, Haider N, Hofmann F, Wegener JW: Mouse models to study L-type calcium channel function. Pharmacol Ther. 2005, 106: 347-355. 10.1016/j.pharmthera.2004.12.003.
Okamura Y, Nakaseko HI, Nakajo K, Ohtsuka Y, Ebihara T: The ascidian dihydropyridine-resistant calcium channel as the prototype of chordate L-type calcium channel. Neurosignals. 2003, 12: 142-158. 10.1159/000072161.
Bosma MM, Moody WJ: Macroscopic and single-channel studies of two Ca2+ channel types in oocytes of the ascidian Ciona intestinalis. J Membr Biol. 1990, 114: 231-243. 10.1007/BF01869217.
Dale B, Talevi R, DeFelice LJ: L- type Ca2+ currents in ascidian eggs. Exp Cell Res. 1991, 192: 302-306. 10.1016/0014-4827(91)90190-6.
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Thanks are due to Dr. GianLuigi Russo for helpful comments and to Mr. Giuseppe Gargiulo for computer graphic.
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Tosti, E. Calcium ion currents mediating oocyte maturation events. Reprod Biol Endocrinol 4, 26 (2006). https://doi.org/10.1186/1477-7827-4-26
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DOI: https://doi.org/10.1186/1477-7827-4-26